Monahan began his musical career singing with cover band Rogues Gallery from 1988 to 1990. The band consisted of Monahan (lead vocals, percussion), Mark Emhoff (lead guitar, vocals), Mike Imboden (bass, keyboards, vocals), John McElhenny (drums, vocals) and his brother Matt McElhenny (rhythm guitar, keyboards and vocals), in his hometown of Erie, Pennsylvania. After the dissolution of the band, he left Erie in late 1993 and moved to California, where he met Rob Hotchkiss. While progressing from the SF coffeehouse circuit to the LA club scene, Monahan and Hotchkiss added Jimmy Stafford (guitar), Charlie Colin (bass), and Scott Underwood (drums) to their lineup, thus officially forming Train.

From 1994 to 2006, Monahan released four studio albums with Train. In 2002, the band earned two Grammys, one of them for the song "Drops of Jupiter (Tell Me)", which was written by Monahan and inspired by his late mother, who had died of cancer.

From 2006 to 2009, Train took a three-year hiatus. Monahan released his first solo album, Last of Seven, on September 18, 2007 and began a nationwide tour supporting it. He followed that tour with a small, intimate acoustic tour, which inspired his Last of Seven Acoustic compilation, available via digital download only. His first solo single, "Her Eyes", made the top 10 of Billboard's Hot AC chart. The album's second single was "Two Ways to Say Goodbye."

In 2009, Train returned to the studio with the critically acclaimed album Save Me, San Francisco. That same year, Monahan and some of his fellow Train bandmates took on small acting roles in the CSI: NY episode "Second Chances". Monahan played the former homeless drug addict Sam Baker (dating Debbie Fallon[4]) who becomes involved in a murder investigation. They performed the song "Hey, Soul Sister" from their new album, and "Calling All Angels".

Monahan also recorded a duet with Martina McBride, singing Train's song "Marry Me". This version of the song is on McBride's eleventh studio album Eleven, released October 11, 2011. He also performed several times with INXS during 2011; first on The Tonight Show with Jay Leno and then at a concert at Chateau Ste Michelle. Monahan also appeared on the show The Voice, where he performed "Drops of Jupiter" with contestant Vicci Martinez.

In 2013, he started a podcast called Patcast where he interviews different people in the music industry, and talks about his work with Train.[5][6]

Monahan is the voice of Driver Dan in the children's show Driver Dan's Story Train, which debuted on Sprout on November 1, 2010.[9] In early 2013, Monahan played the role of Neil Redding in a Season 3 episode of CBS's Hawaii Five-0, titled "Paʻani" ("The Game"), which aired on February 18, 2013.[10] Monahan also played the role of Sam Baker a musician in CSI NY.

Monahan met his second wife, Amber Peterson, during a show on May 14th, 2004.[13] Monahan and Peterson tied the knot on July 20th, 2007.[14] They have two children together: Autumn and Rock Richard.[9][15] They reside in Issaquah, Washington.[16]